SEIPIN proteins mediate lipid droplet biogenesis to promote pollen transmission and reduce seed dormancy

Lipid droplets (LDs) are ubiquitous organelles in plant cells, but their physiological roles are largely unknown. To gain insight into the function of LDs in plants, we have characterized the Arabidopsis homologs of SEIPIN proteins, which are crucial factors for LD biogenesis in yeast and animals. SEIPIN1 is expressed almost exclusively in embryos, while SEIPIN2 and SEIPIN3 have broader expression profiles with maximal levels in embryos and pollen, where LDs accumulate most abundantly. Genetic analysis demonstrates that all three SEIPINs contribute to proper LD biogenesis in embryos, whereas in pollen, only SEIPIN2 and SEIPIN3 play a significant role. The double seipin2 seipin3 and triple seipin mutants accumulate extremely enlarged LDs in seeds and pollen, which hinders their subsequent mobilization during germination. Interestingly, electron microscopy analysis reveals the presence of nuclear LDs attached to type I nucleoplasmic reticulum in triple seipin mutant embryos, supporting that SEIPINs are essential for maintaining the correct polarity of LD budding at the nuclear envelope, restricting it to the outer membrane. In pollen, the perturbations in LD biogenesis and turnover are coupled to reduced germination in vitro and with lower fertilization efficiency in vivo. In seeds, germination per se is not affected in seipin2 seipin3 and triple seipin mutants, but there is a striking increase in seed dormancy levels. Our findings reveal the relevance of SEIPIN-dependent LD biogenesis in pollen transmission and in adjusting the timing of seed germination, two key adaptive traits of great importance in agriculture.